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American Journal of Sports

Medicine
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The Effects of Core Proprioception on Knee Injury: A Prospective Biomechanical-Epidemiological


Study
Bohdanna T. Zazulak, Timothy E. Hewett, N. Peter Reeves, Barry Goldberg and Jacek Cholewicki
Am. J. Sports Med. 2007; 35; 368 originally published online Jan 31, 2007;
DOI: 10.1177/0363546506297909

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The Effects of Core Proprioception
on Knee Injury
A Prospective Biomechanical-Epidemiological Study
Bohdanna T. Zazulak,*†‡§ DPT, MS, OCS, Timothy E. Hewett,||¶ PhD, FACSM,
§# ** §#
N. Peter Reeves, MSc, Barry Goldberg, MD, and Jacek Cholewicki, PhD

From the Department of Rehabilitation Services, Yale New Haven Hospital, New Haven,

Connecticut, Department of Physical Therapy, Quinnipiac University, New Haven, Connecticut,
§
Department of Orthopaedics & Rehabilitation, Biomechanics Research Laboratory, Yale
||
University School of Medicine, New Haven, Connecticut, Sports Medicine Biodynamics Center
and Human Performance Laboratory, Cincinnati Children’s Hospital Research Foundation,

Cincinnati, Ohio, the Departments of Pediatrics, Orthopaedic Surgery, and Biomedical
Engineering and Rehabilitation Sciences, University of Cincinnati College of Medicine,
#
Cincinnati, Ohio, the Department of Biomedical Engineering, Yale University, New Haven,
Connecticut, and **Yale University Health Services, Yale University, New Haven, Connecticut

Background: In sports involving pivoting and landing, female athletes suffer knee injury at a greater rate than male athletes.
Hypotheses: Proprioceptive deficits in control of the body’s core may affect dynamic stability of the knee. Female, but not male,
athletes who suffered a knee injury during a 3-year follow-up period would demonstrate decreased core proprioception at base-
line testing as compared with uninjured athletes.
Study Design: Cohort study (prognosis); Level of evidence, 2.
Methods: Study subjects were 277 collegiate athletes (140 female, 137 male) who were prospectively tested for core proprioception
by active and passive proprioceptive repositioning. Athletes were monitored for injury for 3 years. An ANOVA and multivariate logis-
tic regression were used to test whether core proprioception was related to knee injuries in athletes.
Results: Twenty-five athletes sustained knee injuries (11 women, 14 men). Deficits in active proprioceptive repositioning were
observed in women with knee injuries (2.2º) and ligament/meniscal injuries (2.4º) compared with uninjured women (1.5º, P ≤ .05).
There were no differences in average active proprioceptive repositioning error between injured men and uninjured men (P ≥ .05).
Uninjured women demonstrated significantly less average error in active proprioceptive repositioning than uninjured men (1.5º
vs 1.7º, P ≤ .05). For each degree increase in average active proprioceptive repositioning error, a 2.9-fold increase in the odds
ratio of knee injury was observed, and a 3.3-fold increase in odds ratio of ligament/meniscal injury was observed (P ≤ .01). Active
proprioceptive repositioning predicted knee injury status with 90% sensitivity and 56% specificity in female athletes.
Conclusions: Impaired core proprioception, measured by active proprioceptive repositioning of the trunk, predicted knee injury
risk in female, but not male, athletes.
Keywords: neuromuscular control; proprioception; ACL injury; gender differences; injury prevention

Female athletes have a greater susceptibility to knee greater susceptibility and a 10-fold increase in the female
injury than male athletes.1,7,9,31,38 The combination of this sports population since the inception of Title IX has
resulted in a dramatic increase in the number of knee
*Address correspondence to Bohdanna T. Zazulak, DPT, MS, OCS, injuries in women.31 In the United States, women and girls
Yale New Haven Hospital, Yale Physician’s Building, 800 Howard Avenue,
sustain more than 30 000 anterior cruciate ligament (ACL)
New Haven, CT 06510; e-mail: bohdanna.zazulak@ynhh.org.
Presented at the interim meeting of the AOSSM, San Diego, February injuries a year, with costs that may exceed $650 million
2007. annually.29 The mechanism of ACL injury may include a
No potential conflict of interest declared. combination of the following components: valgus position-
ing of the lower extremity, relative extension with unbal-
The American Journal of Sports Medicine, Vol. 35, No. 3
DOI: 10.1177/0363546506297909
anced weight distribution, and the center of the mass of
© 2007 American Orthopaedic Society for Sports Medicine the body displaced away from the plantar surface of the

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368
Vol. 35, No. 3, 2007 Core Proprioception on Knee Injury 369

foot that is flat on the ground.12,22 Proprioceptive deficits in but not in male athletes. Measurable deficiencies in core
the body’s core may contribute to decreased active neuro- proprioception could identify modifiable neuromuscular
muscular control of the lower extremity, which may lead to risk factors that predispose athletes to knee injury.
valgus angulation and increased strain on the ligaments of
the knee.3,15,19,27,37
METHODS
The core of the body includes the passive structures of
the thoracolumbar spine and pelvis and the active contri-
butions of the trunk musculature.35 The stability of the
body’s core is contingent on neuromuscular control of the Subjects
trunk in response to internal and external forces, including
Subjects were 277 Yale varsity athletes who volunteered
the forces generated from distal body parts and from
for the study. The participants comprised 140 women
expected or unexpected perturbations. Core stability, as
(mean age, 19.4 yrs ± 1.0; mean height, 1.70 m ± 0.08; mean
generally defined in sports medicine literature, is a foun-
body mass, 65.6 kg ± 8.7; mean body mass index, 22.6
dation of trunk dynamic control that allows production,
kg/m2 ± 2.2) and 137 men (mean age, 19.3 yrs ± 1.8; mean
transfer, and control of force and motion to distal segments
height, 1.83 m ± 0.08; mean body mass, 79.9 kg ± 11.9;
of the kinetic chain.20 For the purposes of this study, a more
mean body mass index, 23.8 kg/m2 ± 2.8). Athletes were
precise operational definition was developed. Core stability
tested at baseline and then followed for 3 years to track
was defined as the body’s capacity to maintain or resume a
any knee injuries sustained during that period. Before
relative position of the trunk after perturbation.
experimental testing, every subject completed a detailed,
Deficits in core neuromuscular control may contribute
45-item questionnaire pertaining to personal data (height,
to unstable behavior and injury throughout all segments
weight, and age), athletic experience, varsity level sport(s)
of the kinetic chain.19 For example, abdominal muscle
affiliation, and history of injury. None of the athletes
fatigue appears to contribute to hamstring injuries.10 In
enrolled in the study had any history of knee injury. Knee
agreement with these findings, retrospective studies of
injury was defined as any ligament, meniscal, or
subjects with prior ankle sprains demonstrated a delay in
patellofemoral injury diagnosed by the university sports
the onset of muscle activation of the gluteus maximus6
medicine physician. Fractures and contusions were
and the gluteus medius.2 Cholewicki et al8 observed
excluded from the knee-injured athlete group. Knee
prospectively that delayed trunk muscle reflex responses
injuries were further subclassified as only ligament and/or
predicted low-back injuries in collegiate athletes. A
meniscal, and then only ACL injuries. Athletes were not
recent large prospective cohort study reported that
injured at the time of the test. All ligament and meniscal
female athletes who subsequently suffered an ankle
injuries were confirmed by magnetic resonance imaging
injury demonstrated significantly greater body sway than
(MRI). All subjects understood the experimental protocol
uninjured athletes.4 In contrast, predictors of injury in
and signed the consent form, both of which were approved
male athletes were related to ankle range of motion and
by the Human Investigation Committee.
not measures of proprioception.4 To date, no study has
established a correlation between core neuromuscular
control and knee injury. Proprioception Experiment
Many athletic maneuvers, such as running, jumping,
and cutting, are inherently unstable and require neuro- Core proprioception was evaluated using a previously
muscular control to maintain stability and improve per- validated apparatus as described by Taimela et al (Figure
formance.25,26 Neuromuscular control of the trunk is based 1).23,24,33 The apparatus was designed to produce passive
on feedback control. The information concerning the state motion of the lumbar spine in the transverse plane. Subjects
of the system, such as position of each segment, is fed back were positioned on this apparatus so that the vertical pivot
and used to modify the descending movement commands. axis extended through the L4/L5 vertebrae. The seat was
A host of sensory information is used to track the system driven by a stepper motor at a steady, slow rate to minimize
over time.11 Because control is driven by the estimated tactile cueing. The contribution of the vestibular system was
state and not the true state, accuracy in representation eliminated since the upper body remained fixed to the back-
becomes an issue. A poorly represented system cannot be rest with a 4-point seatbelt and the lower body moved in the
controlled properly and at some point will become unsta- plane parallel to the ground. Care was taken to eliminate
ble. Consequently, impaired core proprioception may lead visual and auditory cues of the apparatus motion. Therefore,
to impaired control of the core, which in turn affects con- this proprioception test focused mainly on the feedback from
trol of the knee and may lead to knee injury. muscular and articular mechanoreceptors of the trunk.
The purpose of this study is to identify potential factors Subjects were initially rotated 20° away from the neu-
related to neuromuscular control of the trunk that predis- tral spine posture (at 2º per second) and briefly held in that
pose athletes to knee injuries. We hypothesize that core position for 3 seconds. In the passive test, the subjects were
proprioception may play a role in dynamic stability of the slowly rotated toward the original position by the motor (at
lower extremity and subsequent knee injuries. The first 1º per second). In the active test, the subject rotated him-
hypothesis is that decreased proprioception will increase self or herself after the clutch was disengaged from
knee injury risk. The second hypothesis is that propriocep- the motor drive. In both tests, the subjects stopped the
tive deficits will predict knee injury risk in female athletes apparatus by pressing a switch when they perceived they

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370 Zazulak et al The American Journal of Sports Medicine

The ANOVA returned a significant interaction between


sex and knee injuries. Deficits in APR were observed in
female subjects with knee (2.2º) and ligament/meniscal
injuries (2.4º) compared with uninjured female subjects
(1.5º, P ≤ .05) (Figure 2). There was no significant difference
in average error in APR between injured male subjects
compared with uninjured male subjects (P ≥ .05) (Figure 2).
Interestingly, uninjured female subjects demonstrated sig-
nificantly less average error in APR than uninjured male
subjects (1.5º vs 1.7º, P ≤ .05) (Figure 2). No difference in
the average error in PPR was observed in knee injured ver-
sus uninjured athletes (P ≥ .05).
For each degree increase in average APR error, a 2.9-fold
increase in the odds ratio of knee injury (P = .005) and 3.3-
fold increase in the odds ratio of ligament/meniscal injury
were observed (P = .007). Active proprioceptive reposition-
ing predicted knee injury status with 90% sensitivity and
56% specificity, and ligament/meniscal injuries with 86%
and 61% specificity in female athletes (Table 2).
Figure 1. An apparatus for testing core proprioception. The
stepper motor drive can be disengaged for active reposition-
ing or engaged for passive repositioning. DISCUSSION

The findings of the current study demonstrate that


increased error in core proprioception is associated with
were in the original, neutral position. Each subject per- increased knee injury risk, which supports our first
formed 4 practice trials before each test, 2 in each direction. hypothesis. The poor APR of the trunk in those female ath-
Subsequently, 5 randomized trials in each direction for letes who subsequently suffered knee injuries supports our
each test were performed. second hypothesis and indicates that decreased core pro-
prioception could alter dynamic knee stability and may
Statistical Analysis explain the increased risk of knee injury during sports
activity in this high-risk population.
The average absolute repositioning errors from all 10 trials The proprioceptive deficits were observed in APR and not
were calculated. To determine the most appropriate set of PPR in the injured female athletes. The active (APR) and
parameters for regression analysis, a 2-factor ANOVA with
Tukey’s post-hoc test was used to identify the measures
that differed significantly between the injured and unin-
jured athletes (P ≤ .05). The 2 factors were as follows: knee
injury versus no knee injury during the follow-up, and male
versus female. The dependent measures were the average
absolute error in active proprioceptive repositioning
(APR) and passive proprioceptive repositioning (PPR). A
prior analysis determined that 21 injuries were required to
achieve an adequate power of 0.8.
The reproducibility of both measures was tested by com-
puting intraclass correlation coefficients (ICC) (2, k)
between the averages of the first 5 trials and the last 5 tri-
als for each of the 277 subjects. The reproducibility of APR
and PPR was good as indicated by the ICC of 0.61 and 0.58,
respectively.

RESULTS

During the 3-year posttest follow-up period, 25 of the 277


athletes sustained knee injuries; 11 occurred in female sub-
jects and 14 in male subjects (Table 1). There were 16 liga- Figure 2. Average absolute error in active proprioceptive
ment and/or meniscal injuries; 7 occurred in women and 9 repositioning in female and male athletes who sustained or
in men. Of these, 11 were ligament injuries. Six subjects did not sustain knee, ligament/meniscal, or anterior cruciate
sustained ACL rupture, 4 females and 2 males. All ACL ligament injury during the follow-up period (*P < .05). Error
injuries were confirmed by MRI. bars designate standard error of the mean.

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Vol. 35, No. 3, 2007 Core Proprioception on Knee Injury 371

TABLE 1
Description of the Injured Athletesa

Classification

Athlete Sex Injury Knee Lig/Men ACL

1 F ACL X X X
2 M ACL/MCL X X X
3 M PF X
4 M MCL X X
5 F ACL/MCL/MEN X X X
6 F PF X
7 M PF X
8 M LCL/MEN X X
9 M PF X
10 F PF X
11 F PF X
12 F PF X
13 F MEN X X
14 M PF X
15 F PF/MEN X X
16 M PF/MEN X X
17 M MEN X X
18 M MCL/MEN X X
19 F ACL/MEN X X X
20 F PF/MEN X X
21 M PF X
22 M MEN X X
23 M ACL/MEN X X X
24 M MCL X X
25 F ACL/MEN X X X
a
Lig/men, ligament and meniscus; MEN, meniscus; ACL, anterior cruciate ligament; F, females; M, males; MCL, medial collateral ligament;
PF, patellofemoral; LCL, lateral collateral ligament.

passive (PPR) tests differ with respect to the relative con- ability than male athletes who did not go on to sustain
tribution of the muscle receptor sensory input. In the knee injury. In addition, the findings of Beynnon et al4
active test, trunk muscles generate the movement and related to ankle injury indicate that women and men have
maintain fusimotor drive, therefore muscle spindle feed- significantly different predictors of injury risk. Body sway
back is involved.11 However, during the passive test, when was reported to be a strong predictor of ankle injury risk
muscles are not active, fusimotor activity and the sensory in female but not male athletes.4 There is no previously
feedback from muscle spindles are decreased. Therefore, published literature to the authors’ knowledge supporting
input from joint and cutaneous receptors likely plays a a relationship between decreased core proprioception and
greater role in sensory feedback.11 Hence, the level of input knee injury. Our prospective study lends greater credence
from the muscle spindles during reproduction of the trunk to this association between decreased neuromuscular con-
position likely differed between the active and passive trol of the body’s core and increased knee injury risk.
tests. The observed deficits in active proprioception may Hewett et al14,16 suggested that dynamic neuromuscular
have been translated to active athletic maneuvers associ- training that enhances control of the body’s core would
ated with knee injuries. improve dynamic stability of the knee joint. Proprioceptive
The second hypothesis is that proprioceptive deficits and neuromuscular control deficits are observed after ACL
would predict knee injury risk in female athletes. We rupture and well into the postoperative rehabilitation
hypothesized that this relationship would not be period. Patients with ACL deficiency have impaired pos-
observed in male athletes for several reasons. First, male tural sway. Women with ACL-deficient knees and after
and female athletes have different ACL injury rates and ACL reconstruction possess greater deficits in propriocep-
potentially different underlying mechanisms of ACL tion and neuromuscular control, as measured by postural
injury.22 Second, our prior data demonstrated that body sway deficits, than their injured and reconstructed male
sway was significantly worse in female subjects who suf- counterparts.16
fered ACL injury than in male subjects who sustained The published literature referencing sex differences in
ACL injury.16 In agreement with these earlier findings, postural sway is equivocal, as 2 other studies reported pos-
the female athletes who did not subsequently suffer tural sway on stable force platforms in healthy subjects
knee injury had significantly better trunk proprioceptive and observed no differences between sexes.5,13 In contrast,

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372 Zazulak et al The American Journal of Sports Medicine

TABLE 2
Results of a Logistic Regression Analysis for Predicting Knee Injuriesa

Women Men

Knee Lig/Men Lig ACL Knee Lig+Men Lig ACL

APR error (P value) 0.006 0.007 – – 0.914 0.852 – –


Odds ratio 2.91 3.31 – – – – – –
Overall P value 0.005 0.007 0.913 0.851
Concordant observations 72.9% 74.0% 38.1% 39.8%
Sensitivity 90% 86% 62% 75%
Specificity 56% 61% 53% 40%
a
Lig/Men, ligament and meniscus; Lig, ligament; ACL, anterior cruciate ligament; APR, active proprioceptive repositioning.

Hewett et al16,17 examined single-leg balance of male con- study cohort of 277 subjects. Therefore, negative findings
trol subjects compared with female control subjects on a relative to ligament and ACL injuries are not reported to
dynamic unstable platform and reported that the female avoid potential beta-type error.
subjects performed significantly better than the male sub- The tests of proprioception in the lumbar spine were con-
jects. However, in the subjects with ACL deficiency, the ducted under relatively artificial conditions and postures.
men had significantly better preoperative performance The pelvis was immobilized to isolate trunk movement.
than the women.16,17 The finding of proprioceptive differ- Most clinical tests of postural sway and proprioception are
ences between sexes raises important issues. First, women performed with the subject balancing on a single leg, which
with intact knees have better single-leg balance than men involves all segments of the lower extremity and trunk. All
with intact knees. This difference is presumed to be attrib- these factors are potential confounding variables relative
utable to the lower center of gravity in female control sub- to isolated core proprioception in these clinical tests.32 In
jects.21 However, after an ACL injury, women seem to contrast, the current reported method is a more direct
experience greater deficits in balance than men.16 In addi- measure of core proprioception.
tion, the return of single-leg balance after ACL reconstruc-
tion is slower in women than in men.16 CONCLUSION
Hewett et al16 pose an important question of whether
female subjects with ACL ruptures possess deficits in bal- Decreased active core proprioception predicted knee injury
ance or postural control before injury, which creates a pre- risk in female athletes. Athletes may be evaluated for
disposition to injury, or the alternative possibility that proprioceptive deficits before competition and targeted
ACL injury is more traumatic to the proprioceptive sys- for specific active neuromuscular training. Interventions
tems of women than men. The findings of the current study that incorporate core neuromuscular training, including
of better active proprioception in healthy female athletes proprioceptive exercises, may significantly reduce knee
compared with healthy male athletes are consistent with injury risk in this high-risk athletic population. Future
previous findings in healthy athletes, where women have a research should focus on neuromuscular training inter-
superior ability to control body sway on a single limb com- ventions specifically targeted to improve core propriocep-
pared to men.16,17 Furthermore, the prospectively meas- tion. Well-controlled, prospective longitudinal studies of
ured proprioceptive deficits exhibited by injured female defined populations of athletes should follow athletes
athletes support the theory that these deficits may predis- through multiple sports seasons to correlate changing core
pose the athlete to knee injury. The possibility that female proprioceptive profiles to injury risk.
athletes with proprioceptive deficits possess a greater
propensity for knee injury suggests the need for pre- ACKNOWLEDGMENT
screening before athletic participation to assess injury
risk. There is strong evidence that neuromuscular control This work was supported by National Institutes of Health
of the trunk and lower extremity can be improved with grants R01-AR049735-03 (TEH) and NIH grant R01-
neuromuscular training.18,28,30,34,36 AR46844 (JC) from the National Institute of Arthritis and
Our study had a relatively low number of injuries, par- Musculoskeletal and Skin Diseases.
ticularly of the ACL. This low subject number may have
potentially precluded our ability to detect poor APR as a
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